Journal of Integrative Agriculture 2016, 15(10): 23362342

Available online at www.sciencedirect.com

ScienceDirect

RESEARCH ARTICLE

Effects of sustained cold and heat stress on energy intake, growth

and mitochondrial function of broiler chickens
ZHANG Shao-shuai*, SU Hong-guang*, ZHOU Ying, LI Xiu-mei, FENG Jing-hai, ZHANG Min-hong
State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193,
P.R.China

Abstract
To study the correlation of broiler chickens with energy intake, growth and mitochondrial function which exposed to sustained
cold and heat stress and to find out the comfortable temperature, 288 broiler chickens (21-day with (74826) g, 144 males
and 144 females) were divided randomly into six temperature-controlled chambers. Each chamber contained six cages
including eight AA broilers per cage, each cage as a repeat. After acclimation for one week (temperature, 21C; relative
humidity, 60%), the temperature of each chamber was adjusted (finished within 1 h) respectively to 10, 14, 18, 22, 26, or
30C (RH, 60%) for a 14-day experimental period. After treatment, gross energy intake (GEI), metabolizable energy intake
(MEI), the ratio of MEI/BW, metabolizability, average daily gain (ADG), the concentration of liver mitochondria protein and
cytochrome c oxidase (CCO) were measured respectively. Our results confirmed that when the temperature over 26C for
14 days, GEI, MEI and CCO activities were decreased significantly (P<0.05), but the concentration of liver mitochondria
protein was increased and metabolizability of broilers was not influenced (P>0.05). Compared with treatment for 14 days,
the ratio of MEI/body weight (BW) were also decreased when the temperature over 26C after temperature stress for 7 days
(P<0.05), meanwhile mitochondrial protein concentration was increased at 10C and CCO activity was not affected (P>0.05).
Additionally at 22C, the ADG reached the maximal value. When kept in uncomfortable temperatures for a long time, the
ADG and CCO activities of broiler were reduced, which was accompanied by mitochondrial hyperplasia. In summary, our
study focused on the performance of broilers during sustained cold and heat environmental temperatures ranging from 10
to 30C. From the point of view of energy utilization, moreover, 22 to 26C is comfortable for 2842 days broilers. And
these could provide the theoretical basis on the high efficient production.
Keywords: broiler chicken, cytochrome c oxidase, energy intake, metabolizability, sustained cold and heat stress

1. Introduction
Received 29 September, 2015 Accepted 3 February, 2016
ZHANG Shao-shuai, E-mail: zss9587@126.com;
SU Hong-guang, E-mail: hongguang.su@163.com;
Correspondence ZHANG Min-hong, E-mail: zmh66@126.com
*
These authors contributed equally to this study.
2016, CAAS. All rights reserved. Published by Elsevier Ltd.
doi: 10.1016/S2095-3119(15)61314-4

Mitochondria are the energy-producing organelles of eukaryotes, they generate ATP via the oxidative phosphorylation
cycle, which consists of five complexes: complex IIV and
F1FO-ATP synthase (Elston et al. 1998; Noji and Yoshida
2001; Brire et al. 2004; Velours et al. 2009; Sharifabadi
et al. 2012). Among the complexes comprising the oxidative
phosphorylation cycle, cytochrome c oxidase (CCO; com-

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ZHANG Shao-shuai et al. Journal of Integrative Agriculture 2016, 15(10): 23362342

plex IV) is the last of the three proton-pumping complexes.

This complex catalyzes the transfer of electrons from reduced cytochrome c to molecular oxygen, which is the final
electron acceptor (Kadenbach et al. 2000; Popovi et al.
2012; Sampedro-Piquero et al. 2013). Thus, mitochondrial
protein concentration and CCO activity can be used as
indicators of mitochondrial function (Li et al. 2001; Rajaei
Sharifabadi et al. 2012), energy production, and energy
utilization in animals.
Researchers have studied the effects of environmental
temperature on the energy metabolism of hens (Barott and
Pringle 1941, 1946; Wheelock et al. 2010; Dozier et al.
2011; Ferreira et al. 2011; Baumgard and Rhoads 2013).
Yang et al. (2010) found that the function of the mitochondrial respiratory chain would be significantly induced when
the broiler chickens under the acute heat stress. Li et al.
(2001) studied the thermogenesis and thermoregulation of
small mammals following cold acclimation for four weeks,
then summaried the different cold adaptive thermogenesis
at different geographical zones. Wang et al. (2006) investigated the effects of different photoperiods on the energy
utilization of root voles, indicating that standard error (SD)
alone is effective in inducing higher thermogenic capacities
and energy intake coupled with lower body mass and body
fat mass in root voles. Zhu et al. (2010) assessed the energy metabolism and thermogenesis of Eothenomys miletus
following a 49-day cold treatment, their results showed that
E. miletus enhanced thermogenic capacity and increased
maintenance cost during cold acclimation, resulting in increased energy intake.
The above works show the changes of energy metabolism and the changes of mitochondrial respiratory chain
under the acute heat stress or cold treatment in animals.
However, there is little information on the effects of both high
and low temperatures on an individual rather separately
used in one study on the energy consumption and utilization
of broiler chickens at the whole body and cellular levels.
The objective of this study was to assess the energy intake,
body weight, mitochondrial protein concentration, and CCO
activity of broiler chickens exposed to 10 to 30C for 14 days.

2. Materials and methods

2.1. Animals and management
In this study, 288 broiler chickens (144 males and 144 females; Arbor Acres, Beijing, China) at 21 days of age, were
assigned to six environmental chambers. Each chamber
contained six cages with eight birds (four males and four
females) per cage (area of 0.8 m0.75 m), and each cage
as a replication. Birds were kept at 22C and 60% relative
humidity (RH) for one week. Following this acclimation pe-

riod, the temperatures of each environmental chamber were

respectively (within 1 h) set to 10, 14, 18, 22, 26, or 30C
while maintaining RH at 60% for 14 days (the accuracy of
the environmental chamber was 1C for temperature and
7% for RH). Body weight (BW) was measured on days
7 and 14 of the experimental period, without restriction of
feed and water; feed intake was measured every day. The
chickens had ad libitum access to feed and water during the
experimental period and 24-h light cycles. Experimental diet
was designed according to the NRC (1994) requirements.
The composition and nutrient levels of the basal diets are
shown in Table 1. Any aspect of the work covered in this
study involved experimental animals has been conducted
with the ethical approval of all relevant bodies.

2.2. Energy intake

Excreta were collected and weighed on days 7 and 14.
Samples (approximately 100 g per cage) of feed and excreta
were oven-dried at 60C to constant weight. The caloric
values of dry feed and excreta were determined with a Parr
6400 oxygen bomb calorimetry (Parr Instrument, USA).
Energy intake expressed as gross energy intake (GEI),
metabolizable energy intake (MEI), and apparent metabolizability of energy (hereafter referred to as metabolizability)
was calculated according to the methods reported by Wang
Table 1 Composition and nutrient levels of the basal diet (asfed basis) (%)
Items
Ingredients
Corn
Soybean meal
Soybean oil
NaCl
Limestone
CaHPO4
DL-Met
Premix1)
Total
Nutrient levels2)
Metabolizable energy (ME, MJ kg1)
Crude protein (CP)
Ca
Available phosphorus (AP)
Lys
Met
Met+Cys
1)

Contents (%)
56.51
35.52
4.50
0.30
1.00
1.78
0.11
0.28
100.00
12.73
20.07
0.90
0.40
1.00
0.42
0.78

Premix provided the following per kg of the diet: VA 10 000 IU,

VD3 3 400 IU, VE 16 IU, VK3 2.0 mg, VB1 2.0 mg, VB2 6.4 mg,
VB6 2.0 mg, VB12 0.012 mg, pantothenic acid calcium 10 mg,
nicotinic acid 26 mg, folic acid 1 mg, biotin 0.1 mg, choline 500
mg, Zn (ZnSO 47H 2O) 40 mg, Fe (FeSO 47H 2O) 80 mg, Cu
(CuSO45H2O) 8 mg, Mn (MnSO4H2O) 80 mg, I (KI) 0.35 mg,
and Se (Na2SeO3) 0.15 mg.
2)
Calculated values.

ZHANG Shao-shuai et al. Journal of Integrative Agriculture 2016, 15(10): 23362342

Six birds (three males and three females) from each chamber (one bird per cage) were euthanasia by decapitation on
days 7 and 14. Liver samples were immediately frozen in
liquid nitrogen and stored at 80C. Hepatic mitochondria
were isolated according to the method reported by Kun
et al. (1978). Mitochondrial protein concentrations were
determined with a commercial kit (Beijing CellChip Biotechnology Co., Ltd., China) based on the Bradford (1976)
method. CCO activity was spectrophotometrically measured
(TU-1810, Pgeneral, Beijing, China) using a commercial kit
(Genmed Scientifics Inc., Shanghai, China). All tests were
operated strictly according to the instruments supplied by
the manufactures.

2.4. Statistical analyses

Data were analyzed by analysis of variance (ANOVA) and
Duncans multiple comparison tests (SAS Inst. Inc., Cary,
NC). Data were expressed as meansSEM. Cage was
considered the experimental unit. Each temperature treatment was represented by six replicate cages. Statistical
significance was set at P<0.05.

3. Results
GEI, MEI, and CCO, the ratio of MEI/BW, average daily
gain (ADG), the concentration of liver mitochondria protein
and metabolizability were measured respectively (Fig. 1).
When the environment temperature was higher than 26C,
both GEI and MEI significantly decreased on day 7 and 14
(P<0.05). On the other hand, there was no significant variance on GEI or MEI on day 7 or 14 under the environment
temperature lower than 22C. On day 14, the value MEI/BW
decreased at the temperature point 18 and 30C (P<0.05)
and plateaued between 18 and 26C. While on day 7, the
decreasing point of MEI/BW was occurring at 26 and 30C

GEI (kcal d1)

900
800
700

bc
a

ab
a

abc
a

7d
14 d
c

600

c
d

500
400

MEI (kcal d1)

700
650
600
550
500
450
400
350
300

10

ab
a

300
200
100
76
75
74
73
72
71
70
69
68
67
66

E 120
110
100
90
80
70
60
50
40

14
18
22
26
Temperature (C)
a

ab

ab

30
7d
14 d

a
b

10

C 400
MEI/BW (kcal kg1 d1)

2.3. Hepatic mitochondria protein concentration and

CCO activity

A
1 000

Metabolizability (%)

et al. (2006). And these methods were modified as the

excreta of chicken was a mixture of fecal and urine, which
were different from that of mammals:
GEI (kJ d1)=Dry matter intake (DMI) (g d1)Energy
content of feed (kJ g1)
MEI (kJ d1)=GEIDry mass of excreta (g d1)Energy
content of excreta (kJ g1)
Metabolizability (%)=MEI/GEI100
Energy intakes expressed as MEI/BW, which can better
reflect energy consumption of the birds, were also compared
among the different temperature treatments (Barott and
Pringle 1946).

ADG (g)

2338

c
c

14
18
22
26
Temperature (C)

30
7d
14 d

ab

10

10

14
18
22
26
Temperature (C)

30

14
18
22
26
Temperature (C)

30

ab
b
c

bc

ab

a
a

7d
14 d

ab

17 d
814 d
c

ab
bc
c

10

14
18
22
26
Temperature (C)

30

Fig. 1 Differences in gross energy intake (GEI; A), metabolizable

energy intake (MEI; B), metabolizable energy intake/body
weight (MEI/BW; C), metabolizability (D) among broilers at
different environmental temperatures, and differences in
average daily gain (ADG; E) among broilers maintained at
different environmental temperatures. Data are expressed as
meansSE. Data points with different letters are significantly
different at the level of P<0.05. The same as below.

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ZHANG Shao-shuai et al. Journal of Integrative Agriculture 2016, 15(10): 23362342

4. Discussion
It should be mentioned that on day 11 of the experimental
period, the 10C chamber malfunctioned; therefore, the temperature treatment was changed to room temperature, which
ranged from 15 to 23C, since then data of this chamber on
day 14 are only for referential use.
The main environmental factor regulating feed intake
is ambient temperature (Ferket and Gernat 2006; zkan
et al. 2010; Willemsen et al. 2011; Lara and Rostagno
2013). Feed intake in chickens is inversely correlated to
environmental temperature (Prince et al. 1961; zkan et al.
2010; Willemsen et al. 2011). The thermoneutral zone
of chickens is the environmental temperature range over
which the internal body temperature is mostly maintained
by heat originating from normal metabolism (Ferket and
Gernat 2006). Under thermoneutral conditions, birds tend to
consume feed to meet their metabolic requirements (Dozier
et al. 2011). If ambient temperature exceeds thermoneutrality, birds reduce their feed intake to minimize metabolic heat
production (Ferket and Gernat 2006; Lara and Rostagno
2013) and lose metabolic heat through evaporation via panting (Reece and Lott 1982), which removes metabolic heat
that would otherwise be available for growth. In addition,
energy requirements are reduced because of the inability to
dissipate heat resulting from the catabolism of amino acids,
active transport, and other metabolic events (Hurwitz et al.
1980). These factors contribute to a reduction in BW. On
the other hand, at low temperatures, birds regulate their
body temperature by elevating their heat production and
this needs expend considerable more energy. May and

Mitochondrial protein
content (mg g1)

14 d

7d
8

7
ab

6
5

ab
abc

ab
b

bc

ab
ab

4
3
2

10

14

18

22

26

30

Temperature (C)

B
COO activity (102 nmol cytochrome
c oxidase min1 mg1 protein)

(P<0.05). The metabolizability data did not have a regular

pattern under the different temperatures on day 7 or 14.
The environment temperature remarkably affected the
ADG of broiler chickens (P<0.05). On both days 17 and
814, with the increasing of temperature from 1022C, the
ADG were slowly increasing, and at the point 22C, the ADG
reached the maximal value. Along with the temperature
further increase, the sharp decline of ADG occurred from
2230C on days 17 and 814. ADG was the lowest at
30C (P<0.05). BW of birds at 30C was also decreased
on day 14 (data not show) (P<0.05).
Mitochondrial protein concentration and CCO activity are
shown in Fig. 2. Protein concentration was lower at 22C
than at 10C on day 7 (P<0.05). However, there was no
significant differences in CCO activity among the different
temperature treatments (P>0.05). On day 14, the temperature maintained at 14 and 30C, the mitochondria protein
concentrations showed higher than those maintained at 10
or 22C (P<0.05). Moreover, CCO activity at 18C is higher
than that at 26C and 30C (P<0.05).

12

10
8

6
4

a
ab
ab

a ab

2
0

10

14

18
22
Temperature (C)

26

30

Fig. 2 Differences in protein concentration (A) and cytochrome

c oxidase (CCO) activity (B) in hepatic mitochondria of broilers
maintained at different environmental temperatures.

Lott (2001) reported a 4% increase in feed consumption as

temperature decreased from 20 to 12C.
In this study, when expressed as a function of BW (MEI/
BW), the energy intake of broilers decreased at 18 and 26C,
suggesting that to maintain a constant body temperature,
birds need to increase their energy intakes at temperatures
lower than 18C and need to reduce their energy intakes at
temperatures higher than 26C. Additionally, GEI and MEI
decrease at 26C, while the energy reduction at 26C does
not affect BW probably because of a lower maintenance
requirement at 26C that could spare some energy for
growth. Studies have reported that the energy requirements
of chicks and turkeys decrease between 12 and 24C, keep
low between 24 and 28C, and increase when the temperature higher than 28C (Hurwitz et al. 1980; Kamely et al.
2015; Pishnamazi et al. 2015). Even though energy intakes
decrease at 26C, the absorptive efficiency of energy is not
affected as no difference are found in metabolizability. Scott
and Balnave (1991) also reported that there are no changes
in metabolizability between pullets exposed to 2535C and
those exposed to 616C.
MEI/BW was not affected at 18C on day 7, however, it
decreased on day 14. Broilers may have adapted to changes in temperatures after day 14 and the energy requirement
for maintenance may not be as high as that during the first

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ZHANG Shao-shuai et al. Journal of Integrative Agriculture 2016, 15(10): 23362342

few days. When laying hens are exposed to high or low environmental temperatures, the general pattern of physiological
response is initially rapid, followed by a plateau, and finally
at a different level compared to that at the previous temperatures (Harrison and Biellier 1969; Melesse et al. 2011;
Felver-Gant et al. 2012; Ogbu et al. 2014). By measuring
fasting metabolic rate after the environmental temperature
increased from 22 to 28C, Shannon and Brown (1969)
reported that the adaptation period for White Leghorn hen
is 312 days, while that for Light Sussex cockerel is slightly
longer. These studies suggest that birds require a certain
adaptation period to an environmental temperature that is
different to their thermoneutral zone.
Moreover, there are intrinsic relation within the temperature, energy metabolism and the 7-day weight gain. An
important point is that, with the changing of temperature,
there is same variation tendency between energy metabolism and average daily gain, which is when the temperature
increased from 10 to 22C, both energy metabolism and
average daily gain increased, while when the temperature
further increased from 22 to 30C, those data shown decreased sharply. This result indicated that the 22C is an
available temperature for chickens growth.
It has been reported that to meet increased energy demands, cells exposed to stress have increased mitochondrial biogenesis and enzymatic activity in the respiratory
chain (Manoli et al. 2007), which is in accordance with the
increased hepatic mitochondrial protein concentration at low
temperatures after 7 and 14 days. Similarly, hepatic mitochondrial CCO activity increased in ducks exposed to low
temperatures (Goglia et al. 1993). However, in this study,
CCO activity was not affected after 7 days, but decreased
after 14 days. This result may be attributed to a rapid increase in CCO activity before day 7 followed by a reduction
in enzymatic activity. According to previous results (Duclos
et al. 2004; Tan et al. 2010), acute or chronic challenges to
mitochondrial homeostasis can induce a dysfunction in the
respiratory chain and decrease ATP synthesis. Yang et al.
(2010) reported that broilers exposed to 35C and (705)%
RH for 3 h have lower hepatic mitochondrial CCO activity
than the control group.

5. Conclusion
The energy requirements for maintaining a constant body
temperature in broiler chickens decreased at temperature
lower than 18C, reached a plateau at 1826C, and decreased when temperature higher than 26C. Additionally
at 22C, the ADG reached the maximal value. Prolonged
periods of exposure to cold or heat stress induce an increase
in mitochondrial protein synthesis; however, mitochondrial
CCO activity was depressed. In addition, broilers main-

tained at 26C had lower energy intakes, in term of energy

conservation on the premise of no harm to meat production,
this temperature would be optimum. However, the reduced
CCO activity at this temperature may be an indicator of
inefficient energy utilization. In summary, our study focus
on the performance of broilers during sustained cold and
heat environmental temperatures ranging from 10 to 30C.
Moreover, our results demonstrate that ambient temperature ranging from 22 to 26C is comfortable for 2842 days
broilers. Further studies should assess whether energy
requirements or growth are affected after longer (longer
than 14 days) periods of exposure.

Acknowledgements
This study was supported by the Key Technologies R&D
Program of China during the 12th Five-Year Plan period
(2012BAD39B02) and the Science and Technology Innovation Team Project of Chinese Academy of Agricultural
Sciences (cxgc-ias-07-2013). The authors also gratefully
acknowledge the financial support by the State Key Laboratory of Animal Nutrition, Ministry of Science and Technology,
China (2004DA125184G1105).

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